Responses to Static Visual Images in Macaque Lateral Geniculate Nucleus: Implications for Adaptation, Negative Afterimages, and Visual Fading

Abstract

Adaptation to static scenes is a familiar and fundamental aspect of visual perception that causes negative afterimages, fading, and many other visual illusions. To establish a foundation for understanding the neuronal bases of such phenomena and to constrain the contributions of retinal versus cortical processing, we studied the responses of neurons in the dorsal lateral geniculate nucleus during and after the presentation of prolonged static visual stimuli. We found that parvocellular (P) cells (the more numerous and color-sensitive pathway) showed response adaptation with a time constant on the order of tens of seconds and that their response after the removal of a visual stimulus lasting 1 min was similar in amplitude and time course to the response evoked by the photographic negative stimulus. Magnocellular (M) cells (the faster-conducting and achromatic pathway) had after responses that were substantially weaker than responses evoked by patterned visual stimuli. This difference points to the existence of an adaptive mechanism in the P-pathway that is absent or impaired in the M-pathway and is inconsistent with full adaptation of photoreceptors, which feed both pathways. Cells in both pathways often maintained a substantial tonic response throughout 1 min stimuli, suggesting that these major feedforward inputs to cortex adapt too slowly to account for visual fading. Our findings suggest that faster-adapting mechanisms in cortex are likely to be required to account for the dynamics of perception during and after the viewing of prolonged static images.

The impact of brief exposure to high contrast on the contrast response of neurons in primate lateral geniculate nucleus

“…1) was 0.039 s (SD 0.019), and for P-cells it was 0.072 s (SD 0.014). The different response of M-and P-cells to stationary patterns is consistent with the idea that different postreceptoral mechanisms provide adaptation in the two pathways (Dreher et al 1976;Hawken et al 1996;McLelland et al 2009;Purpura et al 1990;Yeh et al 1996). The offset of an anti-preferred grating produced discharges with a shorter time constant of the decay, 0.033 s (SD 0.012) in M-cells and 0.056 s (SD 0.012) in P-cells, and for both onset and offset responses the time constants of the M-cells was significantly less than that of P-cells (P Ͻ 0.01; one-tailed Student's t-tests).…”

Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions

“…Nelson (1991a) revealed some suppressive effects in the LGN, but these could not fully explain those in V1 (Nelson 1991b). McLelland and colleagues studied responses to afterimages induced by prolonged presentation of static images and found these decayed much more quickly in cortex (McLelland et al 2010) than in the LGN (McLelland et al 2009). Crowder et al (2006) report similar effects of contrast adaptation in V1 and V2 of cat visual cortex.…”

“…Adaptation effects have been characterized in the retina (e.g., Baccus and Meister 2002;Brown and Maslund 2001;Chander and Chichilnisky 2001;Rieke 2001;Zaghloul et al 2005), lateral geniculate nucleus (LGN; e.g., Camp et al 2009;McLelland et al 2009;Solomon et al 2004), primary visual cortex (e.g., Carandini et al 1997;Crowder et al 2006;Dragoi et al 2000;Felsen et al 2002;Ghisovan et al 2009;Movshon and Lennie 1989;Muller et al 1999;Ohzawa et al 1985;Wissig and Kohn 2012), area MT (e.g., Kohn and Movshon 2004;Krekelberg et al 2006b;Van Wezel and Britten 2002;Yang and Lisberger 2009), and inferotemporal cortex (e.g., Liu et al 2009;Sawamura et al 2006), among many others (for recent reviews see Kohn 2007;Webster 2011).…”

Hour-long adaptation in the awake early visual system

“…lateral geniculate nucleus; thalamocortical; sensory adaptation THE VISUAL SYSTEM IS HIGHLY dynamic, able to scale neuronal responses across several orders of magnitude of mean luminance and to alter tuning specificity based on recent visual experience. Adaptations of neural responses, lasting from seconds (Baccus and Meister 2002;Brown and Masland 2001;Rieke 2001) to minutes (Dragoi et al 2000;Giaschi et al 1993;Hammond et al 1988;McLelland et al 2009;Ohzawa et al 1985;Vautin and Berkley 1977), have been described, with the longest lasting adaption ϳ10 min (Dragoi et al 2000). Yet, the perceptual effects of long-duration adapting stimuli can last considerably longer [see, for example, Dong et al (2014) Here, we describe a novel form of adaptation, following prolonged visual stimulation, in which the spontaneous activity of neurons in the lateral geniculate nucleus (LGN) of awake rabbits is reduced to as little as 10% of pre-adaptation baseline activity levels and slowly recovers over a period of Ͼ1 h. We demonstrate that this adaptation, which is cell specific and retinotopically precise, is accompanied by an increase in the reliability (reduced Fano factor) and detectability [increased area of receiver operator characteristic (ROC) functions] of visual responses and by an increase in the ratio of evoked-tospontaneous firing rates.…”

“…Adaptations of neural responses, lasting from seconds (Baccus and Meister 2002;Brown and Masland 2001;Rieke 2001) to minutes (Dragoi et al 2000;Giaschi et al 1993;Hammond et al 1988;McLelland et al 2009;Ohzawa et al 1985;Vautin and Berkley 1977), have been described, with the longest lasting adaption ϳ10 min (Dragoi et al 2000). Yet, the perceptual effects of long-duration adapting stimuli can last considerably longer [see, for example, Dong et al (2014)].…”